Abstract

Cellular-resolution in vivo fluorescence imaging is a valuable tool for longitudinal studies of retinal function in vision research. Wavefront sensorless adaptive optics (WSAO) is a developing technology that enables high-resolution imaging of the mouse retina. In place of the conventional method of using a Shack-Hartmann wavefront sensor to measure the aberrations directly, WSAO uses an image quality metric and a search algorithm to drive the shape of the adaptive element (i.e. deformable mirror). WSAO is a robust approach to AO and it is compatible with a compact, low-cost lens-based system. In this report, we demonstrated a hill-climbing algorithm for WSAO with a variable focus lens and deformable mirror for non-invasive in vivo imaging of EGFP (enhanced green fluorescent protein) labelled ganglion cells and microglia cells in the mouse retina.

© 2015 Optical Society of America

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2015 (4)

2014 (5)

Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
[Crossref] [PubMed]

O. P. Kocaoglu, R. D. Ferguson, R. S. Jonnal, Z. Liu, Q. Wang, D. X. Hammer, and D. T. Miller, “Adaptive optics optical coherence tomography with dynamic retinal tracking,” Biomed. Opt. Express 5(7), 2262–2284 (2014).
[Crossref] [PubMed]

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

Y. N. Sulai and A. Dubra, “Non-common path aberration correction in an adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express 5(9), 3059–3073 (2014).
[Crossref] [PubMed]

C. Alt, J. M. Runnels, L. J. Mortensen, W. Zaher, and C. P. Lin, “In vivo imaging of microglia turnover in the mouse retina after ionizing radiation and dexamethasone treatment,” Invest. Ophthalmol. Vis. Sci. 55(8), 5314–5319 (2014).
[Crossref] [PubMed]

2013 (4)

J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Vis. Sci. 54(13), 8237–8250 (2013).
[Crossref] [PubMed]

Y. Jian, R. J. Zawadzki, and M. V. Sarunic, “Adaptive optics optical coherence tomography for in vivo mouse retinal imaging,” J. Biomed. Opt. 18(5), 056007 (2013).
[Crossref] [PubMed]

L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
[Crossref] [PubMed]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref] [PubMed]

2012 (5)

2011 (5)

2010 (3)

C. Li, N. Sredar, K. M. Ivers, H. Queener, and J. Porter, “A correction algorithm to simultaneously control dual deformable mirrors in a woofer-tweeter adaptive optics system,” Opt. Express 18(16), 16671–16684 (2010).
[Crossref] [PubMed]

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE 7550, 755019 (2010).
[Crossref]

A. Myronenko and X. Song, “Intensity-based image registration by minimizing residual complexity,” IEEE Trans. Med. Imaging 29(11), 1882–1891 (2010).
[Crossref] [PubMed]

2009 (2)

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci. 50(12), 5872–5879 (2009).
[Crossref] [PubMed]

J. W. Evans, R. J. Zawadzki, S. M. Jones, S. S. Olivier, and J. S. Werner, “Error budget analysis for an Adaptive Optics Optical Coherence Tomography System,” Opt. Express 17(16), 13768–13784 (2009).
[Crossref] [PubMed]

2008 (1)

2007 (4)

2006 (2)

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience 140(1), 123–136 (2006).
[Crossref] [PubMed]

S. Zommer, E. N. Ribak, S. G. Lipson, and J. Adler, “Simulated annealing in ocular adaptive optics,” Opt. Lett. 31(7), 939–941 (2006).
[Crossref] [PubMed]

2002 (3)

W. Sun, N. Li, and S. He, “Large-scale morphological survey of mouse retinal ganglion cells,” J. Comp. Neurol. 451(2), 115–126 (2002).
[Crossref] [PubMed]

L. N. Thibos, R. A. Applegate, J. T. Schwiegerling, R. Webb, and VSIA Standards Taskforce Members. Vision science and its applications, “Standards for reporting the optical aberrations of eyes,” J. Refract. Surg. 18(5), S652–S660 (2002).
[PubMed]

L. Chen, P. Yang, and A. Kijlstra, “Distribution, markers, and functions of retinal microglia,” Ocul. Immunol. Inflamm. 10(1), 27–39 (2002).
[Crossref] [PubMed]

Adler, J.

Ahmad, K.

Alexander, N. S.

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

Alt, C.

C. Alt, J. M. Runnels, L. J. Mortensen, W. Zaher, and C. P. Lin, “In vivo imaging of microglia turnover in the mouse retina after ionizing radiation and dexamethasone treatment,” Invest. Ophthalmol. Vis. Sci. 55(8), 5314–5319 (2014).
[Crossref] [PubMed]

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE 7550, 755019 (2010).
[Crossref]

Applegate, R. A.

L. N. Thibos, R. A. Applegate, J. T. Schwiegerling, R. Webb, and VSIA Standards Taskforce Members. Vision science and its applications, “Standards for reporting the optical aberrations of eyes,” J. Refract. Surg. 18(5), S652–S660 (2002).
[PubMed]

Arathorn, D. W.

Archibald, M. L.

B. C. Chauhan, K. T. Stevens, J. M. Levesque, A. C. Nuschke, G. P. Sharpe, N. O’Leary, M. L. Archibald, and X. Wang, “Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice,” PLoS One 7(6), e40352 (2012).
[Crossref] [PubMed]

Bedggood, P.

Bifano, T. G.

Biss, D. P.

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE 7550, 755019 (2010).
[Crossref]

D. P. Biss, D. Sumorok, S. A. Burns, R. H. Webb, Y. Zhou, T. G. Bifano, D. Côté, I. Veilleux, P. Zamiri, and C. P. Lin, “In vivo fluorescent imaging of the mouse retina using adaptive optics,” Opt. Lett. 32(6), 659–661 (2007).
[Crossref] [PubMed]

Bonora, S.

Booth, M. J.

M. J. Booth, “Adaptive optics in microscopy,” Philos. Trans. A Math Phys. Eng. Sci. 365(1861), 2829–2843 (2007).
[Crossref] [PubMed]

Burns, M. E.

P. Zhang, A. Zam, Y. Jian, X. Wang, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “Multispectral scanning laser ophthalmoscopy combined with optical coherence tomography for simultaneous in vivo mouse retinal imaging,” Proc. SPIE 9307, 93070H (2015).
[Crossref]

R. J. Zawadzki, P. Zhang, A. Zam, E. B. Miller, M. Goswami, X. Wang, R. S. Jonnal, S. H. Lee, D. Y. Kim, J. G. Flannery, J. S. Werner, M. E. Burns, and E. N. Pugh., “Adaptive-optics SLO imaging combined with widefield OCT and SLO enables precise 3D localization of fluorescent cells in the mouse retina,” Biomed. Opt. Express 6(6), 2191–2210 (2015).
[Crossref] [PubMed]

Burns, S. A.

Callaway, E. M.

L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
[Crossref] [PubMed]

Cetin, A. H.

L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
[Crossref] [PubMed]

Chalupa, L. M.

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience 140(1), 123–136 (2006).
[Crossref] [PubMed]

Chauhan, B. C.

B. C. Chauhan, K. T. Stevens, J. M. Levesque, A. C. Nuschke, G. P. Sharpe, N. O’Leary, M. L. Archibald, and X. Wang, “Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice,” PLoS One 7(6), e40352 (2012).
[Crossref] [PubMed]

Chen, D.

S. M. Jones, S. Olivier, D. Chen, S. Joeres, S. Sadda, R. J. Zawadzki, J. S. Werner, and D. T. Miller, “Adaptive optics ophthalmologic systems using dual deformable mirrors,” Proc. SPIE 6467, 64670H (2007).
[Crossref]

Chen, L.

L. Chen, P. Yang, and A. Kijlstra, “Distribution, markers, and functions of retinal microglia,” Ocul. Immunol. Inflamm. 10(1), 27–39 (2002).
[Crossref] [PubMed]

Coombs, J.

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience 140(1), 123–136 (2006).
[Crossref] [PubMed]

Côté, D.

Cua, M.

de Boer, J. F.

Dong, Z.

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

Dubra, A.

Elsner, A. E.

Evans, J. W.

Felberer, F.

Ferguson, D.

Ferguson, R. D.

Flannery, J. G.

Geng, Y.

L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
[Crossref] [PubMed]

J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Vis. Sci. 54(13), 8237–8250 (2013).
[Crossref] [PubMed]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref] [PubMed]

Y. Geng, A. Dubra, L. Yin, W. H. Merigan, R. Sharma, R. T. Libby, and D. R. Williams, “Adaptive optics retinal imaging in the living mouse eye,” Biomed. Opt. Express 3(4), 715–734 (2012).
[Crossref] [PubMed]

Y. Geng, L. A. Schery, R. Sharma, A. Dubra, K. Ahmad, R. T. Libby, and D. R. Williams, “Optical properties of the mouse eye,” Biomed. Opt. Express 2(4), 717–738 (2011).
[Crossref] [PubMed]

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci. 50(12), 5872–5879 (2009).
[Crossref] [PubMed]

Golczak, M.

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

Goswami, M.

Gradowski, M. A.

Gray, D. C.

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci. 50(12), 5872–5879 (2009).
[Crossref] [PubMed]

Greenberg, K. P.

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci. 50(12), 5872–5879 (2009).
[Crossref] [PubMed]

Hammer, D. X.

He, S.

W. Sun, N. Li, and S. He, “Large-scale morphological survey of mouse retinal ganglion cells,” J. Comp. Neurol. 451(2), 115–126 (2002).
[Crossref] [PubMed]

Hitzenberger, C. K.

Hofer, H.

Hunter, J. J.

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref] [PubMed]

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci. 50(12), 5872–5879 (2009).
[Crossref] [PubMed]

Ivers, K. M.

Jakobs, T. C.

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE 7550, 755019 (2010).
[Crossref]

Jian, Y.

Joeres, S.

S. M. Jones, S. Olivier, D. Chen, S. Joeres, S. Sadda, R. J. Zawadzki, J. S. Werner, and D. T. Miller, “Adaptive optics ophthalmologic systems using dual deformable mirrors,” Proc. SPIE 6467, 64670H (2007).
[Crossref]

Jones, S. M.

J. W. Evans, R. J. Zawadzki, S. M. Jones, S. S. Olivier, and J. S. Werner, “Error budget analysis for an Adaptive Optics Optical Coherence Tomography System,” Opt. Express 17(16), 13768–13784 (2009).
[Crossref] [PubMed]

S. M. Jones, S. Olivier, D. Chen, S. Joeres, S. Sadda, R. J. Zawadzki, J. S. Werner, and D. T. Miller, “Adaptive optics ophthalmologic systems using dual deformable mirrors,” Proc. SPIE 6467, 64670H (2007).
[Crossref]

Jonnal, R. S.

Kijlstra, A.

L. Chen, P. Yang, and A. Kijlstra, “Distribution, markers, and functions of retinal microglia,” Ocul. Immunol. Inflamm. 10(1), 27–39 (2002).
[Crossref] [PubMed]

Kim, D. Y.

Kocaoglu, O. P.

Kroisamer, J. S.

Lee, S. H.

Levesque, J. M.

B. C. Chauhan, K. T. Stevens, J. M. Levesque, A. C. Nuschke, G. P. Sharpe, N. O’Leary, M. L. Archibald, and X. Wang, “Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice,” PLoS One 7(6), e40352 (2012).
[Crossref] [PubMed]

Li, C.

Li, N.

W. Sun, N. Li, and S. He, “Large-scale morphological survey of mouse retinal ganglion cells,” J. Comp. Neurol. 451(2), 115–126 (2002).
[Crossref] [PubMed]

Libby, R. T.

Lin, C. P.

C. Alt, J. M. Runnels, L. J. Mortensen, W. Zaher, and C. P. Lin, “In vivo imaging of microglia turnover in the mouse retina after ionizing radiation and dexamethasone treatment,” Invest. Ophthalmol. Vis. Sci. 55(8), 5314–5319 (2014).
[Crossref] [PubMed]

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE 7550, 755019 (2010).
[Crossref]

D. P. Biss, D. Sumorok, S. A. Burns, R. H. Webb, Y. Zhou, T. G. Bifano, D. Côté, I. Veilleux, P. Zamiri, and C. P. Lin, “In vivo fluorescent imaging of the mouse retina using adaptive optics,” Opt. Lett. 32(6), 659–661 (2007).
[Crossref] [PubMed]

Lipson, S. G.

Liu, Z.

Merigan, W. H.

Metha, A.

Miller, D. T.

O. P. Kocaoglu, R. D. Ferguson, R. S. Jonnal, Z. Liu, Q. Wang, D. X. Hammer, and D. T. Miller, “Adaptive optics optical coherence tomography with dynamic retinal tracking,” Biomed. Opt. Express 5(7), 2262–2284 (2014).
[Crossref] [PubMed]

S. M. Jones, S. Olivier, D. Chen, S. Joeres, S. Sadda, R. J. Zawadzki, J. S. Werner, and D. T. Miller, “Adaptive optics ophthalmologic systems using dual deformable mirrors,” Proc. SPIE 6467, 64670H (2007).
[Crossref]

Miller, E. B.

Mortensen, L. J.

C. Alt, J. M. Runnels, L. J. Mortensen, W. Zaher, and C. P. Lin, “In vivo imaging of microglia turnover in the mouse retina after ionizing radiation and dexamethasone treatment,” Invest. Ophthalmol. Vis. Sci. 55(8), 5314–5319 (2014).
[Crossref] [PubMed]

Myronenko, A.

A. Myronenko and X. Song, “Intensity-based image registration by minimizing residual complexity,” IEEE Trans. Med. Imaging 29(11), 1882–1891 (2010).
[Crossref] [PubMed]

Nguyen, H.

J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Vis. Sci. 54(13), 8237–8250 (2013).
[Crossref] [PubMed]

Nuschke, A. C.

B. C. Chauhan, K. T. Stevens, J. M. Levesque, A. C. Nuschke, G. P. Sharpe, N. O’Leary, M. L. Archibald, and X. Wang, “Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice,” PLoS One 7(6), e40352 (2012).
[Crossref] [PubMed]

O’Leary, N.

B. C. Chauhan, K. T. Stevens, J. M. Levesque, A. C. Nuschke, G. P. Sharpe, N. O’Leary, M. L. Archibald, and X. Wang, “Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice,” PLoS One 7(6), e40352 (2012).
[Crossref] [PubMed]

Olivier, S.

S. M. Jones, S. Olivier, D. Chen, S. Joeres, S. Sadda, R. J. Zawadzki, J. S. Werner, and D. T. Miller, “Adaptive optics ophthalmologic systems using dual deformable mirrors,” Proc. SPIE 6467, 64670H (2007).
[Crossref]

Olivier, S. S.

Osakada, F.

L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
[Crossref] [PubMed]

Palczewska, G.

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref] [PubMed]

Palczewski, K.

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref] [PubMed]

Pircher, M.

Porter, J.

Pugh, E. N.

Qi, X.

Queener, H.

Ribak, E. N.

Roorda, A.

Runnels, J. M.

C. Alt, J. M. Runnels, L. J. Mortensen, W. Zaher, and C. P. Lin, “In vivo imaging of microglia turnover in the mouse retina after ionizing radiation and dexamethasone treatment,” Invest. Ophthalmol. Vis. Sci. 55(8), 5314–5319 (2014).
[Crossref] [PubMed]

Sadda, S.

S. M. Jones, S. Olivier, D. Chen, S. Joeres, S. Sadda, R. J. Zawadzki, J. S. Werner, and D. T. Miller, “Adaptive optics ophthalmologic systems using dual deformable mirrors,” Proc. SPIE 6467, 64670H (2007).
[Crossref]

Sarunic, M. V.

Schallek, J.

J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Vis. Sci. 54(13), 8237–8250 (2013).
[Crossref] [PubMed]

Schery, L. A.

Schwiegerling, J. T.

L. N. Thibos, R. A. Applegate, J. T. Schwiegerling, R. Webb, and VSIA Standards Taskforce Members. Vision science and its applications, “Standards for reporting the optical aberrations of eyes,” J. Refract. Surg. 18(5), S652–S660 (2002).
[PubMed]

Sharma, R.

Sharpe, G. P.

B. C. Chauhan, K. T. Stevens, J. M. Levesque, A. C. Nuschke, G. P. Sharpe, N. O’Leary, M. L. Archibald, and X. Wang, “Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice,” PLoS One 7(6), e40352 (2012).
[Crossref] [PubMed]

Sheehy, C. K.

Song, X.

A. Myronenko and X. Song, “Intensity-based image registration by minimizing residual complexity,” IEEE Trans. Med. Imaging 29(11), 1882–1891 (2010).
[Crossref] [PubMed]

Sredar, N.

Stevens, K. T.

B. C. Chauhan, K. T. Stevens, J. M. Levesque, A. C. Nuschke, G. P. Sharpe, N. O’Leary, M. L. Archibald, and X. Wang, “Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice,” PLoS One 7(6), e40352 (2012).
[Crossref] [PubMed]

Sulai, Y.

Sulai, Y. N.

Sumorok, D.

Sun, W.

W. Sun, N. Li, and S. He, “Large-scale morphological survey of mouse retinal ganglion cells,” J. Comp. Neurol. 451(2), 115–126 (2002).
[Crossref] [PubMed]

Tajouri, N.

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE 7550, 755019 (2010).
[Crossref]

Thibos, L. N.

L. N. Thibos, R. A. Applegate, J. T. Schwiegerling, R. Webb, and VSIA Standards Taskforce Members. Vision science and its applications, “Standards for reporting the optical aberrations of eyes,” J. Refract. Surg. 18(5), S652–S660 (2002).
[PubMed]

Tiruveedhula, P.

Tumbar, R.

van der List, D.

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience 140(1), 123–136 (2006).
[Crossref] [PubMed]

Veilleux, I.

Wang, G. Y.

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience 140(1), 123–136 (2006).
[Crossref] [PubMed]

Wang, Q.

Wang, X.

R. J. Zawadzki, P. Zhang, A. Zam, E. B. Miller, M. Goswami, X. Wang, R. S. Jonnal, S. H. Lee, D. Y. Kim, J. G. Flannery, J. S. Werner, M. E. Burns, and E. N. Pugh., “Adaptive-optics SLO imaging combined with widefield OCT and SLO enables precise 3D localization of fluorescent cells in the mouse retina,” Biomed. Opt. Express 6(6), 2191–2210 (2015).
[Crossref] [PubMed]

P. Zhang, A. Zam, Y. Jian, X. Wang, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “Multispectral scanning laser ophthalmoscopy combined with optical coherence tomography for simultaneous in vivo mouse retinal imaging,” Proc. SPIE 9307, 93070H (2015).
[Crossref]

B. C. Chauhan, K. T. Stevens, J. M. Levesque, A. C. Nuschke, G. P. Sharpe, N. O’Leary, M. L. Archibald, and X. Wang, “Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice,” PLoS One 7(6), e40352 (2012).
[Crossref] [PubMed]

Webb, R.

L. N. Thibos, R. A. Applegate, J. T. Schwiegerling, R. Webb, and VSIA Standards Taskforce Members. Vision science and its applications, “Standards for reporting the optical aberrations of eyes,” J. Refract. Surg. 18(5), S652–S660 (2002).
[PubMed]

Webb, R. H.

Werner, J. S.

Williams, D. R.

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
[Crossref] [PubMed]

J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Vis. Sci. 54(13), 8237–8250 (2013).
[Crossref] [PubMed]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref] [PubMed]

Y. Geng, A. Dubra, L. Yin, W. H. Merigan, R. Sharma, R. T. Libby, and D. R. Williams, “Adaptive optics retinal imaging in the living mouse eye,” Biomed. Opt. Express 3(4), 715–734 (2012).
[Crossref] [PubMed]

Y. Geng, L. A. Schery, R. Sharma, A. Dubra, K. Ahmad, R. T. Libby, and D. R. Williams, “Optical properties of the mouse eye,” Biomed. Opt. Express 2(4), 717–738 (2011).
[Crossref] [PubMed]

D. R. Williams, “Imaging single cells in the living retina,” Vision Res. 51(13), 1379–1396 (2011).
[Crossref] [PubMed]

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci. 50(12), 5872–5879 (2009).
[Crossref] [PubMed]

Wolfe, R.

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci. 50(12), 5872–5879 (2009).
[Crossref] [PubMed]

Wong, K. S. K.

Xu, J.

Yang, P.

L. Chen, P. Yang, and A. Kijlstra, “Distribution, markers, and functions of retinal microglia,” Ocul. Immunol. Inflamm. 10(1), 27–39 (2002).
[Crossref] [PubMed]

Yang, Q.

Yin, L.

Zaher, W.

C. Alt, J. M. Runnels, L. J. Mortensen, W. Zaher, and C. P. Lin, “In vivo imaging of microglia turnover in the mouse retina after ionizing radiation and dexamethasone treatment,” Invest. Ophthalmol. Vis. Sci. 55(8), 5314–5319 (2014).
[Crossref] [PubMed]

Zam, A.

Zamiri, P.

Zawadzki, R. J.

P. Zhang, A. Zam, Y. Jian, X. Wang, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “Multispectral scanning laser ophthalmoscopy combined with optical coherence tomography for simultaneous in vivo mouse retinal imaging,” Proc. SPIE 9307, 93070H (2015).
[Crossref]

S. Bonora, Y. Jian, P. Zhang, A. Zam, E. N. Pugh, R. J. Zawadzki, and M. V. Sarunic, “Wavefront correction and high-resolution in vivo OCT imaging with an objective integrated multi-actuator adaptive lens,” Opt. Express 23(17), 21931–21941 (2015).
[Crossref] [PubMed]

R. J. Zawadzki, P. Zhang, A. Zam, E. B. Miller, M. Goswami, X. Wang, R. S. Jonnal, S. H. Lee, D. Y. Kim, J. G. Flannery, J. S. Werner, M. E. Burns, and E. N. Pugh., “Adaptive-optics SLO imaging combined with widefield OCT and SLO enables precise 3D localization of fluorescent cells in the mouse retina,” Biomed. Opt. Express 6(6), 2191–2210 (2015).
[Crossref] [PubMed]

K. S. K. Wong, Y. Jian, M. Cua, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “In vivo imaging of human photoreceptor mosaic with wavefront sensorless adaptive optics optical coherence tomography,” Biomed. Opt. Express 6(2), 580–590 (2015).
[Crossref] [PubMed]

Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
[Crossref] [PubMed]

Y. Jian, R. J. Zawadzki, and M. V. Sarunic, “Adaptive optics optical coherence tomography for in vivo mouse retinal imaging,” J. Biomed. Opt. 18(5), 056007 (2013).
[Crossref] [PubMed]

J. W. Evans, R. J. Zawadzki, S. M. Jones, S. S. Olivier, and J. S. Werner, “Error budget analysis for an Adaptive Optics Optical Coherence Tomography System,” Opt. Express 17(16), 13768–13784 (2009).
[Crossref] [PubMed]

S. M. Jones, S. Olivier, D. Chen, S. Joeres, S. Sadda, R. J. Zawadzki, J. S. Werner, and D. T. Miller, “Adaptive optics ophthalmologic systems using dual deformable mirrors,” Proc. SPIE 6467, 64670H (2007).
[Crossref]

Zhang, P.

Zhou, X.

Zhou, Y.

Zommer, S.

Zou, W.

Biomed. Opt. Express (11)

Y. Geng, A. Dubra, L. Yin, W. H. Merigan, R. Sharma, R. T. Libby, and D. R. Williams, “Adaptive optics retinal imaging in the living mouse eye,” Biomed. Opt. Express 3(4), 715–734 (2012).
[Crossref] [PubMed]

R. J. Zawadzki, P. Zhang, A. Zam, E. B. Miller, M. Goswami, X. Wang, R. S. Jonnal, S. H. Lee, D. Y. Kim, J. G. Flannery, J. S. Werner, M. E. Burns, and E. N. Pugh., “Adaptive-optics SLO imaging combined with widefield OCT and SLO enables precise 3D localization of fluorescent cells in the mouse retina,” Biomed. Opt. Express 6(6), 2191–2210 (2015).
[Crossref] [PubMed]

Y. N. Sulai and A. Dubra, “Non-common path aberration correction in an adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express 5(9), 3059–3073 (2014).
[Crossref] [PubMed]

Y. Geng, L. A. Schery, R. Sharma, A. Dubra, K. Ahmad, R. T. Libby, and D. R. Williams, “Optical properties of the mouse eye,” Biomed. Opt. Express 2(4), 717–738 (2011).
[Crossref] [PubMed]

A. Dubra and Y. Sulai, “Reflective afocal broadband adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express 2(6), 1757–1768 (2011).
[Crossref] [PubMed]

K. S. K. Wong, Y. Jian, M. Cua, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “In vivo imaging of human photoreceptor mosaic with wavefront sensorless adaptive optics optical coherence tomography,” Biomed. Opt. Express 6(2), 580–590 (2015).
[Crossref] [PubMed]

Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
[Crossref] [PubMed]

R. Sharma, L. Yin, Y. Geng, W. H. Merigan, G. Palczewska, K. Palczewski, D. R. Williams, and J. J. Hunter, “In vivo two-photon imaging of the mouse retina,” Biomed. Opt. Express 4(8), 1285–1293 (2013).
[Crossref] [PubMed]

C. K. Sheehy, Q. Yang, D. W. Arathorn, P. Tiruveedhula, J. F. de Boer, and A. Roorda, “High-speed, image-based eye tracking with a scanning laser ophthalmoscope,” Biomed. Opt. Express 3(10), 2611–2622 (2012).
[Crossref] [PubMed]

O. P. Kocaoglu, R. D. Ferguson, R. S. Jonnal, Z. Liu, Q. Wang, D. X. Hammer, and D. T. Miller, “Adaptive optics optical coherence tomography with dynamic retinal tracking,” Biomed. Opt. Express 5(7), 2262–2284 (2014).
[Crossref] [PubMed]

X. Zhou, P. Bedggood, and A. Metha, “Limitations to adaptive optics image quality in rodent eyes,” Biomed. Opt. Express 3(8), 1811–1824 (2012).
[Crossref] [PubMed]

IEEE Trans. Med. Imaging (1)

A. Myronenko and X. Song, “Intensity-based image registration by minimizing residual complexity,” IEEE Trans. Med. Imaging 29(11), 1882–1891 (2010).
[Crossref] [PubMed]

Invest. Ophthalmol. Vis. Sci. (3)

C. Alt, J. M. Runnels, L. J. Mortensen, W. Zaher, and C. P. Lin, “In vivo imaging of microglia turnover in the mouse retina after ionizing radiation and dexamethasone treatment,” Invest. Ophthalmol. Vis. Sci. 55(8), 5314–5319 (2014).
[Crossref] [PubMed]

J. Schallek, Y. Geng, H. Nguyen, and D. R. Williams, “Morphology and topography of retinal pericytes in the living mouse retina using in vivo adaptive optics imaging and ex vivo characterization,” Invest. Ophthalmol. Vis. Sci. 54(13), 8237–8250 (2013).
[Crossref] [PubMed]

Y. Geng, K. P. Greenberg, R. Wolfe, D. C. Gray, J. J. Hunter, A. Dubra, J. G. Flannery, D. R. Williams, and J. Porter, “In vivo imaging of microscopic structures in the rat retina,” Invest. Ophthalmol. Vis. Sci. 50(12), 5872–5879 (2009).
[Crossref] [PubMed]

J. Biomed. Opt. (1)

Y. Jian, R. J. Zawadzki, and M. V. Sarunic, “Adaptive optics optical coherence tomography for in vivo mouse retinal imaging,” J. Biomed. Opt. 18(5), 056007 (2013).
[Crossref] [PubMed]

J. Comp. Neurol. (1)

W. Sun, N. Li, and S. He, “Large-scale morphological survey of mouse retinal ganglion cells,” J. Comp. Neurol. 451(2), 115–126 (2002).
[Crossref] [PubMed]

J. Neurophysiol. (1)

L. Yin, Y. Geng, F. Osakada, R. Sharma, A. H. Cetin, E. M. Callaway, D. R. Williams, and W. H. Merigan, “Imaging light responses of retinal ganglion cells in the living mouse eye,” J. Neurophysiol. 109(9), 2415–2421 (2013).
[Crossref] [PubMed]

J. Opt. Soc. Am. A (1)

J. Refract. Surg. (1)

L. N. Thibos, R. A. Applegate, J. T. Schwiegerling, R. Webb, and VSIA Standards Taskforce Members. Vision science and its applications, “Standards for reporting the optical aberrations of eyes,” J. Refract. Surg. 18(5), S652–S660 (2002).
[PubMed]

J. Vis. (1)

A. Roorda, “Adaptive optics for studying visual function: a comprehensive review,” J. Vis. 11(5), 6 (2011).
[Crossref] [PubMed]

Nat. Med. (1)

G. Palczewska, Z. Dong, M. Golczak, J. J. Hunter, D. R. Williams, N. S. Alexander, and K. Palczewski, “Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye,” Nat. Med. 20(7), 785–789 (2014).
[Crossref] [PubMed]

Neuroscience (1)

J. Coombs, D. van der List, G. Y. Wang, and L. M. Chalupa, “Morphological properties of mouse retinal ganglion cells,” Neuroscience 140(1), 123–136 (2006).
[Crossref] [PubMed]

Ocul. Immunol. Inflamm. (1)

L. Chen, P. Yang, and A. Kijlstra, “Distribution, markers, and functions of retinal microglia,” Ocul. Immunol. Inflamm. 10(1), 27–39 (2002).
[Crossref] [PubMed]

Opt. Express (5)

Opt. Lett. (3)

Philos. Trans. A Math Phys. Eng. Sci. (1)

M. J. Booth, “Adaptive optics in microscopy,” Philos. Trans. A Math Phys. Eng. Sci. 365(1861), 2829–2843 (2007).
[Crossref] [PubMed]

PLoS One (1)

B. C. Chauhan, K. T. Stevens, J. M. Levesque, A. C. Nuschke, G. P. Sharpe, N. O’Leary, M. L. Archibald, and X. Wang, “Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice,” PLoS One 7(6), e40352 (2012).
[Crossref] [PubMed]

Proc. SPIE (3)

P. Zhang, A. Zam, Y. Jian, X. Wang, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “Multispectral scanning laser ophthalmoscopy combined with optical coherence tomography for simultaneous in vivo mouse retinal imaging,” Proc. SPIE 9307, 93070H (2015).
[Crossref]

C. Alt, D. P. Biss, N. Tajouri, T. C. Jakobs, and C. P. Lin, “An adaptive-optics scanning laser ophthalmoscope for imaging murine retinal microstructure,” Proc. SPIE 7550, 755019 (2010).
[Crossref]

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[Crossref]

Vision Res. (1)

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[Crossref] [PubMed]

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[Crossref]

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Supplementary Material (1)

NameDescription
» Visualization 1: MP4 (5809 KB)      A video of the change in the appearance of the ganglion cell during the optimization process as displayed on the screen.

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Figures (7)

Fig. 1
Fig. 1

Schematic of the WSAO f/c biomicroscope using 488 nm excitation from an Ar/Kr laser. Relay lenses are achromatic doublets. Other optical elements: 80/20 beam splitter (BS), dichroic mirror (DC), deformable mirror (DM), zero-order quarter wave plate (QWP), objective lens (OBJ), linear polarizer (LP), pinhole (PH), variable lens (VL), galvanometer scanning mirrors (GM). Electronic elements: avalanche photo diode (APD), photo multiplier tube (PMT). The images on the computer icon are representative images of the structural and fluorescence imaging channels.

Fig. 2
Fig. 2

WSAO modal hill-climbing algorithm flowchart for the fluorescence image optimization process; deformable mirror (DM), variable lens (VL).

Fig. 3
Fig. 3

US Air Force resolution target with line width 2.19 µm highlighted by the red rectangle to demonstrate the reflectance resolution. Scale bar: 50 µm.

Fig. 4
Fig. 4

Images of 2.1 µm diameter fluorescent beads acquired a) before WSAO optimization and b) after optimization. c) The line plots for a bead before and after optimization. Scale bars: 10 µm.

Fig. 5
Fig. 5

a,b) Ganglion cells labelled by EGFP comparing the images acquired before and after the WSAO optimization. These images are an average of 50 frames of an off-axis ganglion cell. Scale bars: 20 µm.

Fig. 6
Fig. 6

a) The Zernike coefficients applied to the DM (deformable mirror) after the optimization. b) The impact of the optimization on the intensity-based merit function are plotted for each mode. The intensity is normalized from zero when the DM is flat. The Zernike coefficients are reported by the OSA standard for optical aberrations of eyes [28]. c) The intensity plot of a dendrite on the EGFP-labelled ganglion cell at the location and in the direction indicated by the arrows.

Fig. 7
Fig. 7

Images of EGFP-labelled retinal microglia cells acquired in vivo before and after WSAO correction with different field of views: a, b, and c. Images b) and c) were taken at the same location with different field of views as indicated by the red dashed box. Each image is an average of 50 frames. Scale bars: 10 µm.

Equations (2)

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J(k)= x,y I w(k) (x,y) ,
w(k)= n=3 20 k n Z n .

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